Abstract

In the wake of the end-Permian mass extinction, the Early Triassic (~251.9 to 247 million years ago) is portrayed as an environmentally unstable interval characterized by several biotic crises and heavily depauperate marine benthic ecosystems. We describe a new fossil assemblage—the Paris Biota—from the earliest Spathian (middle Olenekian, ~250.6 million years ago) of the Bear Lake area, southeastern Idaho, USA. This highly diversified assemblage documents a remarkably complex marine ecosystem including at least seven phyla and 20 distinct metazoan orders, along with algae. Most unexpectedly, it combines early Paleozoic and middle Mesozoic taxa previously unknown from the Triassic strata, among which are primitive Cambrian-Ordovician leptomitid sponges (a 200–million year Lazarus taxon) and gladius-bearing coleoid cephalopods, a poorly documented group before the Jurassic (~50 million years after the Early Triassic). Additionally, the crinoid and ophiuroid specimens show derived anatomical characters that were thought to have evolved much later. Unlike previous works that suggested a sluggish postcrisis recovery and a low diversity for the Early Triassic benthic organisms, the unexpected composition of this exceptional assemblage points toward an early and rapid post-Permian diversification for these clades. Overall, it illustrates a phylogenetically diverse, functionally complex, and trophically multileveled marine ecosystem, from primary producers up to top predators and potential scavengers. Hence, the Paris Biota highlights the key evolutionary position of Early Triassic fossil ecosystems in the transition from the Paleozoic to the Modern marine evolutionary fauna at the dawn of the Mesozoic era.

Keywords

End-Permian mass extinction

biotic recovery

Early Triassic

marine ecosystems

Idaho

Paris Biota

INTRODUCTION

The Permian-Triassic boundary (PTB) [~251.9 million years ago (Ma)] is characterized by the largest Phanerozoic mass extinction, marking the end of the dominance of the Sepkoski’s Paleozoic evolutionary fauna and the expansion of the Modern evolutionary fauna (1). The PTB and subsequent Early Triassic recovery interval are characterized by recurrent marked changes in water temperature (2, 3), large-scale fluctuations of the global carbon cycle, and harsh marine conditions including a combination of ocean acidification, anoxia, euxinia, and fluctuating productivity (Fig. 1) (4–6).

The postcrisis biotic recovery was rapid for some nektonic-pelagic groups, such as ammonoids and conodonts (7, 8). In contrast, delayed, spatially heterogeneous recovery of species-poor communities is assumed to be the hallmark of benthic ecosystems (9–16).

Until now, the oldest known marine Mesozoic complex ecosystem was dated from the Middle Triassic of China (Luoping biota, ~242 Ma) (17). Here, we report a new, exceptionally well-preserved and diversified Early Triassic marine biota from Paris, southeastern Idaho, USA (see Figs. 1 to 3 and the Supplementary Materials). Ammonoid and conodont biostratigraphy indicates an earliest Spathian (middle Olenekian, ~250.6 Ma) (Fig. 1) (5) age for this biota and is therefore the first and oldest known Early Triassic complex marine ecosystem.

(A) Present-day map showing the location of southeastern Idaho in western United States. (B) Map of southeastern Idaho showing the location of the Paris Biota. (C) Early Triassic map with the location of the Paris Biota. (A) to (C) were modified following the study by Romano et al. (57).

Fig. 3Simplified stratigraphic log showing main Early Triassic fossil-bearing levels currently known in the Bear Lake area.

Fossil occurrence is modified following the study by Romano et al. (57), with additional data from studies by Massare and Callaway (58) (ichthyosaur remains), Tosk and Andersson (59) (foraminifers), and Hofmann et al. (60) and from our own field observations (black stars). Conodonts are also sparsely present throughout the section but are not represented here. Stratigraphy follows the main units defined by Kummel (61, 62). Zonation is based on ammonoids (20, 54, 55, 62, 63). Position of the Paris Biota is highlighted in red. A U-Pb age of 250.55 ± 0.4 My is associated with the Tirolites/Columbites beds from South China (5). LL, Lower Limestone; LS, Lower Shale; ML, Middle Limestone; MS, Middle Shale; UCS, Upper Calcareous Siltstone; Meek, Meekoceras beds; Anasib, Anasibirites beds; Tirol, Tirolites beds; Colum, Columbites beds.

The earliest Spathian represents a time of transition following a severe late Smithian extinction event (Fig. 1) (7, 8). During the Early Triassic recovery, the middle Smithian and late Smithian were subject to renewed, large-scale perturbations of the global biogeochemical cycles (4–6, 18), including some of the largest δ13C excursions of the Phanerozoic, and a peak in seawater temperatures (Fig. 1) (2, 3). In low latitudes, these high temperatures, along with anoxia, are hypothesized to have been lethal to many marine clades (2). The newly discovered Paris Biota (named herein) is therefore highly unexpected because it documents a markedly diversified benthic ecosystem only ~1.3 million years (My) after the PTB in an equatorial setting.

Exposures and sampled material

The Paris Biota was found in four neighboring and equivalent exposures of the upper part of the early Spathian Lower Shale unit of the Early Triassic Thaynes Group [sensu Lucas et al. (19)], west of the city of Paris, Idaho (see Figs. 2 and 3, figs. S1 and S2, and the Supplementary Materials). The alternating limestones and shales of the Thaynes Group reflect deposition within the relatively shallow western U.S. basin. During the Early Triassic, it was located at a near-equatorial position on the western margin of Pangea (Fig. 2C). Tirolites ammonoid specimens are found throughout the four studied exposures of the upper part of the Lower Shale unit, confirming an earliest Spathian age for this biota (see the Supplementary Materials).

Compared to previously described Early Triassic assemblages [for example, see study by Schubert and Bottjer (9)], the Paris Biota shows a remarkably high diversity (Figs. 4 to 6, figs. S3 and S4, and table S1) with abundant sponges, brachiopods, bivalves, ammonoids, belemnoids, arthropods, and fishes. Ammonoids and bivalves dominate the biota in terms of abundance, as is normally observed in Smithian and Spathian fossil levels from the western U.S. basin (13, 20). Crinoids, ophiuroids, orthoconic nautiloids, gladius-bearing coleoids, fishes, algae, and vertebrate coprolites also occur. Overall, more than 750 individuals (excluding isolated fossil pieces and fragments) representing at least seven phyla and >20 orders have been collected so far (Figs. 4 to 6, figs. S3 to S28, and table S1). Some of these organisms are documented from the Early Triassic for the first time (leptomitid sponges and gladius-bearing coleoids), and several display anatomical characters that were thought to have evolved much later (for example, echinoderms), indicating an early and rapid post-PTB diversification for these groups as well as previously unknown phylogenetical links between Paleozoic and Mesozoic taxa.

There is no major faunal difference between the four sampled exposures, suggesting similar ecological conditions and depositional settings. Macroscopic field observations and thin section analyses indicate that a part of the sedimentary succession was formed by storm-mobilized sediments. Abundant planar and undulated laminae indicate an outer shelf in the deepest part of the storm-dominated environments (that is, 60 to 100 m below sea level; see the Supplementary Materials). The completeness of delicate specimens, especially echinoderms and crustaceans, demonstrates that they were usually entombed rapidly and close to their original habitat. There is no evidence of any size-sorting, mixing, or reworking processes. Rarity of infaunal bioturbation, high sedimentation rate, and abundance of framboidal and polyhedral pyrite suggest upper sediment dysoxic to anoxic conditions. However, the seafloor was oxygenated, as testified by the abundance of benthic organisms including crinoids and ophiuroids, which require well-oxygenated conditions.

Ammonoid, sponge, arthropod, and brachiopod specimens are usually flattened. Most other fossils are compressed but preserve some three-dimensional features (Figs. 4 to 6 and figs. S5 to S28). Contrary to some Middle Triassic assemblages preserving soft parts [for example, see study by Hu et al. (17)], no evidence of microbial mat–enhanced preservation was found. Mollusks (except gladius-bearing coleoids) and echinoderms are preserved in calcite. Sponges, arthropods, brachiopods, and coprolites are preserved in calcium phosphate (figs. S29 to S33), suggesting rapid decay and burial in phosphatizing microenvironments. Phosphatic preservation is common for coprolites, vertebrate remains, cuticle of crustaceans, and coleoid soft parts (21) but rare for sponges [for example, see study by Castellani et al. (22)]. Belemnoid hooks and parts of gladius-bearing coleoids are preserved as carbonaceous structures (fig. S32).

RESULTS

The Paris Biota is highly diversified and shows a largely unexpected composition. It combines taxa usually found in the Early Triassic from the western U.S. basin (for example, ammonoids, nautiloids, bivalves, lingulids, ophiuroids, and vertebrates) with more unusual taxa and with others previously unknown for this time interval (leptomitid sponges, epizoan brachiopods, crinoids, gladius-bearing coleoids, belemnoids, arthropods, and algae) (Figs. 4 to 6 and figs. S5 to S28). In this remarkable biota, leptomitid protomonaxonids (Figs. 4, A and B, and 5 and figs. S5 to S11) are by far the most unexpected taxon. Although isolated spicules and specimens of Early Triassic siliceous and hypercalcified sponges are frequently found in the western U.S. basin (23–28), all complete sponge specimens recovered from the Paris Biota belong to the leptomitid protomonaxonids. These sponges differ markedly from all other sponge taxa reported so far from the Early Triassic, including the western U.S. basin (24–26). In particular, they show a weak and delicate structure characterized by primarily longitudinal spicules, a helical twisting of the skeleton, and a fringe of spicules projecting from the apex to form marginalia (Fig. 5 and figs. S5 to S11). These features are typical of leptomitid protomonaxonids and are unknown from other sponge groups, including the morphologically plastic, often ecophenotypically variable demosponges. Convergence with any other sponge group can therefore be confidently discarded, including the grossly reminiscent modern hexactinellid sponge Euplectella aspergillum, whose skeleton is primarily made of a fused (as adults), orthogonally reticulate grid that is reinforced by diagonal (helical) bundles and an oscular sieve plate (see the Supplementary Materials) (29). Leptomitid protomonaxonids are phylogenetically distant from extant siliceous sponges and are most typical of Sepkoski’s Cambrian evolutionary fauna (1), most particularly of the Cambrian Burgess Shale–type faunas, although these protomonaxoids are also present in lower abundance in some Ordovician deposits with exceptional preservation (30–32). Some Silurian faunas may be dominated by protomonaxonids but without clear links to older faunas (30). Very few protomonaxonids from later Paleozoic rocks and no examples of Leptomitidae are known. Therefore, the Paris Biota sponges represent a Lazarus taxon with a ~200-My gap in the fossil record, highlighting the poor resolution of the fossil record for this group (30). Long ghost lineages for surviving Cambrian-type sponges are also known elsewhere, including a Late Triassic calcareous sponge genus previously restricted to the Cambrian (33). The minute epizoan brachiopods (Figs. 4B and 5C and fig. S13) occasionally found in close association with these leptomitid sponges directly echo similar biotic associations described in early Paleozoic biotas (34, 35), suggesting that this brachiopod-sponge association also survived ~200 My longer than previously thought. Furthermore, these specimens indicate that Early Triassic brachiopods exploited not only seafloor habitats but also additional tiering levels above the substratum.

New forms of the articulate crinoid order Holocrinida are documented for the first time in the Early Triassic, with most skeletal elements articulated (Figs. 4H and 6H and figs. S22 and S23). We collected two proximal stems with cirri, and subcomplete isolated arms. These fossils display advanced characters (for example, presence of cryptosymplectial articulations; see the Supplementary Materials), indicating an intense morphological diversification before or during the earliest Spathian, much earlier than previously thought (36, 37). Ophiuroid remains include one complete specimen, which is considerably larger than previously known Early Triassic ophiuroids (Fig. 4I and figs. S24 and S25) (38, 39). The diagnostic skeletal characters (for example, spine articulations) suggest basal ophiodermatid affinities, thus pushing the origin of the ophiodermatid clade and the early ophiuroid diversification to the lower limits of divergence time estimates (40, 41).

We also report the unexpected occurrence of gladius-bearing coleoids (Fig. 4G and fig. S17). Previously unknown in Early Triassic strata, gladius-bearing coleoids diversified during the Jurassic and the Cretaceous [for example, see study by Fuchs and Larson (42)]. The specimens reported here demonstrate that these gladius-bearing coleoids already existed by the Early Triassic. A putative representative of this clade was recently described from the Early Permian (43) but with a gladius morphology completely distinct from Mesozoic ones. Proostracum-bearing coleoids are classically considered as the most likely ancestors of gladius-bearing coleoids (44). Nevertheless, regardless of the still-unknown phylogenetic relationships between Permian and Triassic taxa, the microlaminated ultrastructure and organic composition of the Paris Biota gladii suggest that gladius-bearing coleoids did not evolve from proostracum-bearing coleoids. Instead, they indicate an independent evolution of these clades from a still-unknown late Paleozoic common ancestor (see the Supplementary Materials).

Hundreds of mostly isolated belemnoid arm hooks have also been recovered (Fig. 6, A and B, and fig. S16). Similar forms were already described from a Spitsbergen Spathian locality (45); thus, their occurrence in the Paris Biota is not surprising per se, although their high abundance is notable. The size of these hooks suggests that their bearers were about 15 to 20 cm long, corresponding to middle-sized predators. Their abundance and stratigraphic recurrence indicate a stable presence and high life abundance of these predators in the earliest Spathian of this area. In addition, hook concentrations observed in some coprolites (Fig. 6, K and L) demonstrate that these active predators were consumed by even larger vertebrate predators (fishes or reptiles), the fossils of which are known from the same area (see Fig. 6, I and J, and the Supplementary Materials).

At least five taxa of arthropods are present in the Paris Biota (Figs. 4, C to F, and 6, C to F). These include two new genera of thylacocephalans, an uncommon and enigmatic group of arthropods (Fig. 4D and fig. S21). This is the first reported occurrence of thylacocephalans from Triassic rocks in North America, considerably extending their spatiotemporal distribution (46). In addition, the Paris Biota yields the richest fauna of Triassic crustaceans found so far in North America, with abundant decapods including glyphidean lobsters and caridean and penaeid shrimps [Figs. 4, C to F, and 6, C to F, and figs. S18 to S21].

Last, algae are represented by rod-shaped and branching morphotypes showing potential affinities with noncalcified dasycladales and other late Paleozoic green algae, respectively (Fig. 6G and fig. S28). They cover large surfaces at some horizons, suggesting transient blooms. These indicate that algae may have been important primary producers in some Early Triassic trophic networks. The Early Triassic diversity, abundance, and geographic distribution of these fragile organisms (especially when noncalcified) remain largely unknown.

DISCUSSION

Overall, the Paris Biota illustrates a diversified and trophically complete marine ecosystem—from primary producers up to top predators and potential scavengers (see figs. S3 to S28 and the Supplementary Materials). It is close in complexity to the Middle Triassic Luoping biota (17), which has classically been viewed as an iconic example of a post-PTB fully rediversified marine ecosystem. This is all the more notable given the fact that the Paris Biota lived in the immediate aftermath of the end-Smithian extinction event in an equatorial setting, that is, at a time and place where marine ecosystems are thought to be heavily depauperate (2).

The unexpected co-occurrence of taxa previously known only in early Paleozoic or in middle-to-late Mesozoic strata demonstrates that some Early Triassic ecosystems were much more phylogenetically diverse and functionally much more complex than previously thought. The Paris Biota illustrates the oldest occurrence of derived characters in several clades (fig. S3), and it shows that at least some Early Triassic marine communities include ancient lineages in the lowest trophic levels together with newly evolved groups occupying higher trophic levels.

By revealing previously hidden ecosystem complexity and unexpected taxonomic occurrences that increase global Early Triassic biodiversity, this remarkable biota constitutes a new landmark for understanding the marine recovery dynamics after the end-Permian mass extinction. It stands in stark contrast with previous works that suggested a sluggish recovery and low diversity of marine benthic organisms during the Early Triassic (9, 10). The Paris Biota shows that functionally complex, trophically multileveled marine ecosystems were actually present soon (~1.3 My) after the end-Permian mass extinction, at least in some areas that may have acted as biotic refugia. However, its peculiar composition indicates that its high diversity is not the simple consequence of a rapid post-PTB diversification. Instead, it represents the combined effect of the maintenance of long-ranging Paleozoic taxa and the early appearance of derived clades whose minimum age of origination is pre-Spathian (see the Supplementary Materials). The detailed timing of this faunal transition remains unknown because Lagerstätten (that is, sites of exceptional preservation) are extremely rare in the Permian-Triassic interval and they provide only a few macroevolutionary calibration points. The frequent low-diversity benthic assemblages commonly sampled in Early Triassic rocks were shown to have a biased composition for some major benthic clades (15, 25). They might therefore represent poorly sampled, taxonomically biased subsets of much more diversified ecosystems resembling the Paris Biota, at least at the level of the western U.S. basin. Alternatively, the Paris Biota may actually represent an assemblage whose taxonomic and functional diversity results from peculiar biotic and environmental conditions acting at the local scale. Additional field data from correlative beds and different depositional environments are required before general conclusions can be drawn on the spatiotemporal distribution of the Paris Biota. Nevertheless, this finding illustrates that the Late Permian–Early Triassic fossil record remains incompletely known for many marine higher-level taxa, even in the intensively studied western U.S. basin that is probably one of the best studied areas in the world for this time interval. Consequently, conclusions of a uniform recovery at the basin scale are no more supportable on the basis of currently available evidences, than would be a simple recovery model at the global scale.

Revealing the link between community composition and recovery dynamics will be critical in understanding the transition from the Paleozoic to the Modern evolutionary faunas. The Paris Biota highlights the key evolutionary position of Early Triassic fossil ecosystems in the transition from the Paleozoic to the Modern biosphere and that the rise of the Modern evolutionary fauna at least sometimes emerged from taxonomically, phylogenetically, and ecologically diverse communities.

MATERIALS AND METHODS

The four exposures studied are located near the city of Paris, southeastern Idaho (see Fig. 2 and the Supplementary Materials). More than 750 (sub)complete individual specimens (excluding isolated fossil pieces and fragments) were collected from these exposures so far. Figured specimens were housed in the collections of the Université de Bourgogne (Dijon, France) and the Idaho Museum of Natural History (Pocatello, USA). Specimens were observed in natural light using a Leica M205C binocular microscope coupled with a Leica DFC295 digital camera. Photographs were taken in natural light and UV light (365 nm) using a Nikon D5300 reflex camera and processed in Adobe Photoshop CS5. A camera lucida attached to Leica M205C was used for interpretative drawings. Scanning electron microscope (SEM) observations coupled with energy-dispersive spectrometer (EDS) analyses were performed at the Institut Carnot de Bourgogne (Dijon, France) to determine the elemental composition of fossil fragments. Variably oriented thin sections were also prepared and observed in natural and polarized light microscopy using a Nikon AZ100 microscope coupled with a digital camera.

SUPPLEMENTARY MATERIALS

fig. S1. Field view of the upper part of the Lower Shale unit containing the Paris Biota.

fig. S2. Log section of the main Paris Biota exposure.

fig. S3. Taxa of the Paris Biota showing unexpected or extended temporal distributions, new Early Triassic spatiotemporal occurrences, new oldest records of derived characters for the clade, and new ecologic or trophic interactions.

fig. S4. Artistic reconstruction of the Paris Biota.

fig. S5. Closeup view of an apex of a leptomitid protomonaxonid sponge.

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Acknowledgments: We thank H. Hagdorn, L. E. Holmer, A. H. Knoll, A. Pisera, T. M. Scheyer, and D. Vachard for discussion. L.J.K. thanks C. Powell for assistance in the field. We acknowledge the Bear Lake County Road department and D. M. Clow (Ogden) for allowing access to the studied exposures. We also thank the reviewers for their constructive comments. Funding: This work is a contribution to the Agence Nationale de la Recherche projects AFTER (ANR-13-JS06-0001-01) and EvoDevOdonto (ANR-14-ACHN-0010). Author contributions: Fieldwork was carried out by A.B., L.J.K., J.F.J., K.G.B., E.F., E.V., N.O., N.G., D.A.S, and G.E. Thin section studies were performed by E.V. and N.O. Determinations of ammonoids: A.B., J.F.J., and K.G.B.; nautiloids: A.B.; belemnoid hooks: A.B. and K.G.B.; gladius-bearing coleoids: L.D.; sponges: J.P.B.; crinoids: T.S.; ophiuroids: B.T.; arthropods: S.C.; brachiopods: A.B.; bivalves: M.H.; conodonts: N.G.; other vertebrate remains: C.R.; algae: A.B. and G.E. All authors contributed to the discussion. A.B., E.F., N.G., E.V., and G.E. wrote the paper, with contribution from all other authors. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Figured specimens were housed at the Université de Bourgogne, Dijon, France, and at the Idaho Museum of Natural History, USA.